Skip to main content
Log in

Selection and characterization of Argentine isolates of Trichoderma harzianum for effective biocontrol of Septoria leaf blotch of wheat

  • Original Paper
  • Published:
World Journal of Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Species of the genus Trichoderma are economically important as biocontrol agents, serving as a potential alternative to chemical control. The applicability of Trichoderma isolates to different ecozones will depend on the behavior of the strains selected from each zone. The present study was undertaken to isolate biocontrol populations of Trichoderma spp. from the Argentine wheat regions and to select and characterize the best strains of Trichoderma harzianum by means of molecular techniques. A total of 84 out of the 240 strains of Trichoderma were able to reduce the disease severity of the leaf blotch of wheat. Thirty-seven strains were selected for the reduction equal to or greater than 50 % of the severity, compared with the control. The percentage values of reduction of the pycnidial coverage ranged between 45 and 80 %. The same last strains were confirmed as T. harzianum by polymerase chain reaction amplification of internal transcribed spacers, followed by sequencing. Inter-simple sequence repeat was used to examine the genetic variability among isolates. This resulted in a total of 132 bands. Further numerical analysis revealed 19 haplotypes, grouped in three clusters (I, II, III). Shared strains, with different geographical origins and isolated in different years, were observed within each cluster. The origin of the isolates and the genetic group were partially related. All isolates from Paraná were in cluster I, all isolates from Lobería were in cluster II, and all isolates from Pergamino and Santa Fe were in cluster III. Our results suggest that the 37 native strains of T. harzianum are important in biocontrol programs and could be advantageous for the preparation of biopesticides adapted to the agroecological conditions of wheat culture.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  Google Scholar 

  • Annone J, Calzalori O, Polidoro H, Conta H (1991) Efecto de la mancha de la hoja causada por Septoria tritici sobre el rendimiento. INTA EEA Pergamino Informe 122:4

    Google Scholar 

  • Ashrafizadeh A, Etebarian H, Zamanizadeh H (2002) Evaluation of Trichoderma isolates in controlling Fusarium wilt of melon. Iran J Plant Pathol 41:39–57

    Google Scholar 

  • Benitez T, Rincón AM, Limón MC, Codon AC (2004) Biocontrol mechanisms of Trichoderma strains. Int Microbiol 7:249–260

    CAS  Google Scholar 

  • Consolo VF, Mónaco CI, Cordo CA, Salerno GL (2012) Characterization of novel Trichoderma spp. isolates as a search for effective biocontrollers of fungal diseases of economically important crops in Argentina. World J Microbiol Biotechnol 28:1389–1398

    Article  CAS  Google Scholar 

  • Cordo CA, Monaco CI, Segarra CI, Simon MR, Mansilla AY, Perelló AE, Conde RD (2007) Trichoderma spp. as elicitors of wheat plant defense responses against Septoria tritici. Biocontrol Sci Technol 17:687–698

    Article  Google Scholar 

  • Cordo C, Simón MR, Stocco M, Lampugnani G, Abramoff C, Kripelz N, Mónaco C (2012) Aplicaciones de Trichoderma harzianum y su efecto sobre las curvas de progreso de la Septoriosis del trigo y el rendimiento. In Abstract of XIV Jornadas Fitosanitarias Argentinas. Section F93

  • Cumagun CJR, Hockenhull J, Lϋbeck M (2000) Characterization of Trichoderma isolates from Philippine rice fields by UP-PCR and rDNA-ITS1 analysis: identification of UP-PCR markers. Phytopathology 148:109–115

    Article  CAS  Google Scholar 

  • De Meyer G, Bigirimana J, Elad Y, Hofte M (1998) Induced systemic resistance in Trichoderma harzianum T39 biocontrol of Botrytis cinerea. Eur J Plant Pathol 104:279–286

    Article  Google Scholar 

  • Dodd SL, Hill RA, Stewart A (2004) A duplex-PCR bioassay to detect a Trichoderma virens biocontrol isolate in non-sterile soil. Soil Biol Biochem 36:1955–1965

    Article  CAS  Google Scholar 

  • Druzhinina IS, Komon-Zelazowska M, Atanasova L, Seidl V, Kubicek CP (2010) Evolution and ecophysiology of the industrial producer Hypocrea jecorina (Anamorph Trichoderma reesei) and a new sympatric agamospecies related to it. PLoS One 5(2):e9191

    Article  Google Scholar 

  • Elad Y, Chet I, Henis I (1981) A selective medium for improving quantitative isolation of Trichoderma sp. from soil. Phytoparasitica 71:59–67

    Article  Google Scholar 

  • Engelberth J, Koch T, Schçûler G, Bachmann N, Rechtenbach J, Boland W (2001) Ion channel-forming alamethicin is a potent elicitor of volatile biosynthesis and tendril coiling. Cross talk between jasmonate and salicylate signaling in lima bean. Plant Physiol 125:369–377

    Article  CAS  Google Scholar 

  • Gherbawy YA, Hussein NA, Al-Qurashi AA (2014) Molecular characterization of Trichoderma populations isolated from soil of Taif City, Saudi Arabia. Int J Curr Microbiol Appl Sci 3(9):1059–1071

    CAS  Google Scholar 

  • Góes LB, Bolena A, Lopes L, Freire DC (2002) Randomly amplified polymorphic DNA of Trichoderma isolates and antagonism against Rhizoctonia solani. Braz Arch Biol Techn 45:151–160

    Article  Google Scholar 

  • Grondona I, Hermosa R, Tejada M, Gomis M, Mateos P, Bridge P, Monte E, Garcia-Acha I (1997) Physiological and biochemical characterization of Trichoderma harzianum, a biological control agent against soilborne fungal plant pathogens. Appl Environ Microbiol 63:3189–3198

    CAS  Google Scholar 

  • Haggag WM (2008) Biotechnological aspects of plant resistant for fungal diseases management, American-Eurasian. J Sustain Agric 2:1–18

    Google Scholar 

  • Hajieghrari B, Torabi-Giglou M, Mohammadi MR, Davari M (2008) Biological potential of some Iranian Trichoderma isolates in control of soil borne plant pathogenic fungi. Afr J Biotechnol 7(8):967–972

    Google Scholar 

  • Harman G (2000) Myths and dogmas of biocontrol: changes in perceptions derived from research on Trichoderma harzianum strain T-22. Plant Dis 84:377–393

    Article  Google Scholar 

  • Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species-opportunistic, avirulent pant symbionts. Nat Rev Microbiol 2:43–56

    Article  CAS  Google Scholar 

  • Hermosa MR, Keck E, Chamorro I, Rubio B, Sanz L, Vizcaíno J, Monte E (2004) Genetic diversity shown in Trichoderma biocontrol isolates. Mycol Res 108(8):897–906

    Article  CAS  Google Scholar 

  • Howell CR (2003) Mechanisms employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts. Plant Dis 87:4–10

    Article  Google Scholar 

  • Howell CR, Hanson LE, Stipanovic RD, Puckhaber LS (2000) Induction of terpenoid synthesis in cotton roots and control of Rhizoctonia solani by seed treatment with Trichoderma virens. Phytopathology 90:248–252

    Article  CAS  Google Scholar 

  • Kraan G, Nisi JE (1993) Septoriosis of wheat in Argentina. Situation of the crop against the disease. P1-8. In: L Gilchrist et al (ed) Proceedings of the Septoria tritici. Workshop, CIMMYT, Mexico City, Mexico, pp 20–24

  • Kumar M, Sharma P (2011) Molecular and morphological characters: an appurtenance for antagonism in Trichoderma spp. Afr J Biotechnol 10(22):4532–4543

    Google Scholar 

  • Lorito M, Woo SL, Harman GE, Monte E (2010) Translational research on Trichoderma: from omics to the field. Annu Rev Phytopathol 48:395–418

    Article  CAS  Google Scholar 

  • Lovell DJ, Parker SR, Hunter T, Royle DJ, Coker RR (1997) Influence of crop growth and structure on the risk of epidemics by Mycosphaerella graminicola (anamorph Septoria tritici) in winter wheat. Plant Pathol 46:126–138

    Article  Google Scholar 

  • Mónaco C, Perelló A, Rollán C (1994) Ensayos “in vitro” del comportamiento antagónico de Trichoderma spp. frente a especies patógenas de la zona hortícola platense. Microbiología SEM 10:423–428

    Google Scholar 

  • Mónaco C, Sisterna M, Perelló A, Dal Bello G (2004) Preliminary studies on biological control of the blackpoint complex of wheat in Argentina. World J Microbiol Biotechnol 20:285–290

    Article  Google Scholar 

  • Monte E (2001) Understanding Trichoderma: between biotechnology and microbial ecology. Int Microbiol 4:1–4

    CAS  Google Scholar 

  • Montero-Barrientos M, Hermosa R, Cardoza RE, Gutiérrez S, Monte E (2011) Functional analysis of the Trichoderma harzianum nox1 gene, encoding an NADPH oxidase, relates production of reactive oxygen species to specific biocontrol activity against Pythium ultimum. Appl Environ Microbiol 77:3009–3016

    Article  CAS  Google Scholar 

  • Moreno MV, Stenglein SA, Balatti PA, Perelló AE (2008) Pathogenic and molecular variability among isolates of Pyrenophora tritici-repentis, causal agent of tan spot of wheat in Argentina. Eur J Plant Pathol 122:239–252

    Article  Google Scholar 

  • Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325

    Article  CAS  Google Scholar 

  • Muthumeenakshi S, Brown AE, Mills PR (1998) Genetic comparison of the aggressive weed mold strains of Trichoderma harzianum from mushroom composts in North America and the British Isles. Mycol Res 102:385–390

    Article  CAS  Google Scholar 

  • Muthumeenakshi S, Mills PR (1995) Detection and differentiation of fungal pathogens of Agaricus bisporus. Mush Sc 14:603–610

    Google Scholar 

  • Ospina-Giraldo MD, Royse DJ, Chen X, Romaine CP (1999) Molecular phylogenetic analyses of biological control strains of Trichoderma harzianum and other biotypes of Trichoderma spp associated with mushroom green mold. Phytopathology 89:308–313

    Article  CAS  Google Scholar 

  • Otadoh JA, Okoth SA, Ochanda J, Kahindi JP (2011) Assessment of Trichoderma isolates for virulence efficacy on Fusarium oxysporum f. sp. phaseoli. Trop Subtrop Agroecosyst 13:99–107

    Google Scholar 

  • Perelló A, Mónaco C, Cordo C (1997) Evaluation of Trichoderma harzianum and Gliocladium roseum in controlling leaf blotch of wheat (Septoria tritici) under in vitro and greenhouse conditions. Z Pflanzenk Pflanzen 104:588–598

    Google Scholar 

  • Perelló A, Mónaco C, Moreno MV, Cordo C, Simón MR (2006) The effect of Trichoderma harzianum and T. koningii on the control of tan spot (Pyrenophora tritici-repentis) and leaf blotch (Mycosphaerella graminicola) of wheat under field conditions in Argentina. Biocontrol Sci Technol 16:803–813

    Article  Google Scholar 

  • Perelló A, Mónaco C, Sisterna M, Dal Bello G (2003) Biocontrol efficacy of Trichoderma isolates for tan spot wheat in Argentina. Crop Prot 22:1099–1106

    Article  Google Scholar 

  • Perelló A, Moreno V, Mónaco C, Simón MR, Cordo C (2009) Biological control of Septoria tritici blotch of wheat by Trichoderma spp under field conditions in Argentina. Biocontrol 54:113–122

    Article  Google Scholar 

  • Perelló A, Simón MR, Arambarri AM, Cordo CA (2001) Greenhouse screening of the saprophytic resident microflora for control of leaf spots of wheat (Triticum aestivum). Phytoparasitica 29:341–351

    Article  Google Scholar 

  • Quiroz-Sarmiento VR, Ferrera-Cerrato R, Alarcón A, Lara-Hernadez ME (2008) Antagonismo in vitro de cepas de Aspergillus y Trichoderma hacia hongos filamentosos que afectan el cultivo de ajo. Rev Mex Micología 26:27–34

    Google Scholar 

  • Rabeendran N, Jone EE, Moot DJ, Stewart A (2006) Biocontrol of Sclerotinia lettuce drop by Coniothyrium minitans and Trichoderma hamatum. Biol Control 39:352–362

    Article  Google Scholar 

  • Rivera M, Wright ER (2014) Control biológico de enfermedades de plantas en Argentina In: Bettiol W, Rivera MC, Mondino P, Montealegre JR, Colmenárez YC (eds) Control biológico de enfermedades de plantas en América Latina y el Caribe, pp 9–81

  • Rohlf FJ (1998) NTSYS-pcVersion 2.0 Numerical taxonomy and multivariate analysis system Setauket. Software, NY

  • Rotblat B, Enshell-Seijffers D, Gershoni JM, Schuster S, Avni A (2002) Identification of an essential component of the elicitation active site of the EIX protein elicitor. Plant J 32:1049–1055

    Article  CAS  Google Scholar 

  • Samson RA (1995) Constraints associated with taxonomy of biocontrol fungi. Can J Bot 73:83–88

    Article  Google Scholar 

  • Samuels GJ, Chaverri P, Farr DF, McCray EB (2013) Trichoderma online, systematic mycology and microbiology laboratory, ARS, USDA. http://nt.ars-grin.gov/taxadescriptions/keys/TrichodermaIndex.cfm. Verified Oct 24 2013

  • Seidl V, Seibel C, Kubicek CP, Schmoll M (2009) Sexual development in the industrial workhorse Trichoderma reesei. Proc Natl Acad Sci USA 106:13909–13914

    Article  CAS  Google Scholar 

  • Sharma K, Mishra AK, Misra RS (2009) Morphological, biochemical and molecular characterization of Trichoderma harzianum isolates for their efficacy as biocontrol agents. J Phytopathol 157:51–56

    Article  CAS  Google Scholar 

  • Simón MR, Perelló AE, Cordo CA, Struik PC (2002) Influence of Septoria tritici blotch (Mycosphaerella graminicola) on yield, yield components and test weight of wheat under two nitrogen fertilisation conditions. Crop Sci 42:1974–1981

    Article  Google Scholar 

  • Sneath PHA, Sokal RR (1973) Numerical taxonomy. The principles and practice of numerical classification. WH Freeman, San Francisco

    Google Scholar 

  • Stenglein SA, Balatti PA (2006) Genetic diversity of Phaeoisariopsis griseola in Argentina as revealed by pathogenic and molecular markers. Physiol Mol Plant Pathol 68:158–167

    Article  CAS  Google Scholar 

  • Stocco M, Consolo F, Mónaco C, Kripelz N, Salerno GL, Cordo C (2012) Control biológico de la mancha de la hoja del trigo con especies del genero Trichoderma. In: Cereales de Invierno II Jornada Temática del INBA “La investigación científico-técnica en cereales de Invierno”. Universidad Nacional del Centro. Buenos Aires, Argentina, p 288

  • Stocco M, Mónaco C, Cordo C (2010) A comparison of preservation methods for Trichoderma harzianum cultures. Rev Iberoam Micol 27:213

    Article  Google Scholar 

  • Stocco M, Mónaco C, Kripelz N, Segarra C, Lampugnani G, Abramoff C, Laporte G, Arteta N, Cordo C (2009) Mecanismo de acción de Trichoderma spp. para el biocontrol de la Septoriosis del trigo. In Abstract of XIII Jornadas Fitosanitarias Argentinas, Octubre de 2009, p 89

  • Stubbs RW, Prescott JM, Saari EE, Dubin HJ (1986) Manual de metodología sobre las enfermedades de Cereales. CIMMYT Mexico

  • Viterbo A, Wiest A, Brotman Y, Chet I, Kenerley C (2007) The 18mer peptaibols from Trichoderma virens elicit plant defence responses. Mol Plant Pathol 8:737–746

    Article  CAS  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, New York, pp 315–322

    Google Scholar 

  • Yap IV, Nelson RJ (1996) WinBoot: a program for performing bootstrap analysis of binary data to determine the confidence limits of UPGMA-based dendrograms., IRRI discussion paper series no 14International Rice Research Institute, Manila

    Google Scholar 

  • Zadoks JC, Chang TT, Konzak CF (1974) A decimal code for the growth stages of cereals. Weed Res 14:415–421

    Article  Google Scholar 

  • Ziv O, Sacks JM, Eyal Z (1981) Inheritance to tolerance to Septoria leaf blotch of wheat. Phytopathology 71:119–123

    Article  Google Scholar 

Download references

Acknowledgments

M. Stocco is a fellow of Consejo Nacional de Investigaciones Científicas y Técnicas, (CONICET) Argentina, V.F Consolo and GL, Salerno are career investigator of CONICET, and C. I. Mónaco and C. A. Cordo are career investigators of Comisión de Investigaciones Científicas Prov. Buenos Aires (CIC), Argentina. This project was supported by CIC of Buenos Aires, Exps. 578-3090/8, 578-1096/10, 2157-1535/11, 2157-2410/2.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Marina C. Stocco.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Stocco, M.C., Mónaco, C.I., Abramoff, C. et al. Selection and characterization of Argentine isolates of Trichoderma harzianum for effective biocontrol of Septoria leaf blotch of wheat. World J Microbiol Biotechnol 32, 49 (2016). https://doi.org/10.1007/s11274-015-1989-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11274-015-1989-9

Keywords

Navigation